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Revisiting pericarp structure, dehiscence and seed dispersal in Galipeeae (Zanthoxyloideae, Rutaceae)

  • Structural Botany - Original Article
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Abstract

Rutaceae is a large family, particularly variable in fruits which have traditionally been used in the delimitation of infrafamilial taxa. Within the family, tribe Galipeeae stands out due to the high diversity of fruits with an exceptional complexity of structure and development, as well as various strategies of seed and fruit dispersal. To better understand the morphological evolution of the tribe, we selected distinct types of fruits occurring in Erythrochiton (subtribe Galipeinae), Esenbeckia, Helietta and Metrodorea (subtribe Pilocarpinae) and comparatively analyzed their structure and development under light microscopy. Erythrochiton has a follicarium, Esenbeckia and Metrodorea capsules, and Helietta a samarium. All species investigated have multiplicative pericarp, resulting in large fruits containing many layers of fibers in the endocarp. The follicarium and capsules grow equally by diffuse cell divisions, but the samarium grows more markedly in the median dorsal part of mericarps, forming wings associated with an aerenchyma, which reduces their specific weight, facilitating dispersal by wind. The loculicidal capsules open along a dorsal dehiscence line, while the ventricidal follicles of the follicarium open along the ventral slit directed by the ventral vascular bundle. Both loculicidal capsules and follicaria dehisce explosively, and the seeds are ejected by the endocarp, which detaches from the pericarp. In addition to the novel observations in Galipeeae, a correlation between the degree of carpel union and the timing of schizocarpy is suggested for the first time.

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References

  • Afonso LF (2018) Ontogenia de frutos em Galipeeae (Rutoideae, Rutaceae). Master’s thesis, Universidade de São Paulo, Ribeirão Preto

  • Albuquerque BWP (1976) Revisão taxonômica das Rutaceae do Estado do Amazonas. Acta Amaz 6:5–67

    Article  Google Scholar 

  • APG Iv - Angiosperm Phylogeny Group (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20

    Article  Google Scholar 

  • Appelhans MS, Bayly MJ, Heslewood MM, Groppo M, Verboom GA, Forster PI, Kallunki JA, Duretto MF (2021) A new subfamily classification of the Citrus family (Rutaceae) based on six nuclear and plastid markers. Taxon. https://doi.org/10.1002/tax.12543

    Article  Google Scholar 

  • Barroso GM, Morin MP, Peixoto AL, Ichaso CLF (1999) Frutos e sementes. Morfologia aplicada à sistemática de dicotiledôneas. Editora UFV, Viçosa

  • Bobrov AVFC, Romanov MS (2019) Morphogenesis of fruits and types of fruit of angiosperms. Bot Lett 166:366–399

    Article  Google Scholar 

  • Brito LA, Dias P, Pirani JR (2019) Synonymization of the monotypic genus Nycticalanthus in Spiranthera (Rutaceae: Galipeinae). Phytotaxa 422:106–108

    Article  Google Scholar 

  • Brückner C (1991) Fruchtanatomische Studien an Dictamnus albus L., Zanthoxylum simulans Hance, Ptelea trifoliata L. und Ruta graveolens L. (Rutaceae). Feddes Repert 102:541–570

    Article  Google Scholar 

  • Bruniera CP, Kallunki JA, Groppo M (2015) Almeidea A St.-Hil. belongs to Conchocarpus J.C. Mikan (Galipeinae, Rutaceae): Evidence from morphological and molecular data, with a first analysis of subtribe Galipeinae. PLoS ONE 10:e0125650

    Article  PubMed  CAS  Google Scholar 

  • Bruniera CP, Silva CI, Groppo M (2011) A new species of Almeidea (Galipeinae, Galipeeae, Rutaceae) from Eastern Brazil. Brittonia 63:281–285

    Article  Google Scholar 

  • Cole TCH, Groppo M (2020) Rutaceae phylogeny poster. ResearchGate. https://www.researchgate.net/publication/324647641. Accessed 10 Jan 2021

  • Colli-Silva M, Pirani JR (2019) Biogeographic patterns of Galipeinae (Galipeeae, Rutaceae) in Brazil: Species richness and endemism at different latitudes of the Atlantic Forest “hotspot.” Flora 251:77–87

    Article  Google Scholar 

  • Cronquist A (1981) An integrated system of classification of flowering plants. Columbia University Press, New York

    Google Scholar 

  • Dias P, Udulutsch RG, Pirani JR (2013) A new species of Metrodorea (Rutaceae) from Brazil: Morphology, molecular phylogenetics, and distribution. Phytotaxa 117:35–41

    Article  Google Scholar 

  • El Ottra JHL (2014) Estrutura floral de Galipeinae (Rutaceae) e suas implicações na sistemática, evolução e biologia do grupo. Ph.D. dissertation, Universidade de São Paulo, São Paulo

  • El Ottra JHL, Demarco D, Pirani JR (2019) Comparative floral structure and evolution in Galipeinae (Galipeeae: Rutaceae) and its implications at different systematic levels. Bot J Linn Soc 191:30–101

    Article  Google Scholar 

  • El Ottra JHL, Pirani JR, Endress PK (2013) Fusion within and between whorls of floral organs in Galipeinae (Rutaceae): structural features and evolutionary implications. Ann Bot 111:821–837

    Article  PubMed  PubMed Central  Google Scholar 

  • Emmerich M (1978) Contribuição ao conhecimento da tribo Cusparineae (Rutaceae): nova conceituação de Raputia e gêneros derivados. Rodriguésia 30:223–307

    Google Scholar 

  • Engler A (1931) Rutaceae. In: Engler A, Prantl K (eds) Die Natürlichen Pflanzenfamilien, vol 19a, 2nd edn. Engelmann, Leipzig, pp 187–359

    Google Scholar 

  • Fernandez-Hilario R, Arteaga R (2017) A new species of Raputia (Rutaceae) from the Selva Central of Peru. PhytoKeys 89:73–84

    Article  Google Scholar 

  • Gerlach D (1984) Botanische Mikrotechnik: eine Einführung, 3rd edn. Georg Thieme, Stuttgart

    Google Scholar 

  • Groppo M, Kallunki JA, Pirani JR, Antonelli A (2012) Chilean Pitavia more closely related to Oceania and Old World Rutaceae than to Neotropical groups: evidence from two cpDNA non-coding regions, with a new subfamilial classification of the family. PhytoKeys 19:9–29

    Article  Google Scholar 

  • Groppo M, Kallunki JA, Pirani JR (2005) Synonymy of Hortia arborea with H. brasiliana (Rutaceae) and a new species from Brazil. Brittonia 57:28–34

    Article  Google Scholar 

  • Groppo M, Pirani JR (2005) Two new species of Hortia (Rutaceae) from Amazonia. Novon 15:139–143

    Google Scholar 

  • Groppo M, Pirani JR (2012) A revision of Hortia (Rutaceae). Syst Bot 37:197–212

    Article  Google Scholar 

  • Groppo M, Pirani JR, Salatino MLF, Blanco SL, Kallunki JA (2008) Phylogeny of Rutaceae based on two noncoding regions from cpDNA. Am J Bot 95:985–1005

    Article  CAS  PubMed  Google Scholar 

  • Gut BJ (1966) Beiträge zur Morphologie des Gynoeceums und der Blütenachse einiger Rutacen. Bot Jahrb Syst 85:151–247

    Google Scholar 

  • Hartl D (1957) Struktur und Herkunft des Endokarps der Rutaceen. Beitr Biol Pflanz 34:35–49

    Google Scholar 

  • Hartl D (1958) Die Übereinstimmung des Endokarps der Simaroubaceen, Rutaceen und Leguminosen. Beitr Biol Pflanz 34:453–455

    Google Scholar 

  • Hertel RJG (1959) Contribuições para a fitologia teórica II. Algumas Concepções Na Carpologia Humanitas 4:11–48

    Google Scholar 

  • Huang LJ, Fu WL (2021) A water drop-shaped slingshot in plants: geometry and mechanics in the explosive seed dispersal of Orixa japonica (Rutaceae). Ann Bot 127:765–774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York

    Google Scholar 

  • Kaastra RC (1982) Pilocarpinae (Rutaceae). Flora Neotrop 33:1–197

    Google Scholar 

  • Kallunki JA (1990) An emended description of and new combinations in Raputia (Cuspariinae, Rutaceae). Brittonia 42:175–177

    Article  Google Scholar 

  • Kallunki JA (1994) Revision of Raputia Aubl. (Cuspariinae, Rutaceae). Brittonia 46:279–295

    Article  Google Scholar 

  • Kallunki JA (1992) A revision of Erythrochiton sensu lato (Cuspariinae, Rutaceae). Brittonia 44:107–139

    Article  Google Scholar 

  • Kallunki JA (1998a) Andreadoxa flava (Rutaceae, Cuspariinae): A new genus and species from Bahia, Brazil. Brittonia 50:59–62

    Article  Google Scholar 

  • Kallunki JA (1998b) Revision of Ticorea Aubl. (Rutaceae, Galipeinae). Brittonia 50:500–513

    Article  Google Scholar 

  • Kallunki JA (2009) Validation of Neoraputia (Galipeae, Rutaceae) and description of two new species from Eastern Brazil. Brittonia 61:28–34

    Article  Google Scholar 

  • Kallunki JA, Pirani JR (1998) Synopses of Angostura and Conchocarpus (Rutaceae). Kew Bull 53:257–334

    Article  Google Scholar 

  • Kubitzki K, Kallunki JA, Duretto M, Wilson PG (2011) Rutaceae. In: Kubitzki K (ed) Flowering plants. Eudicots: Sapindales, Cucurbitales, Myrtaceae. Springer, Heidelberg, pp 276–356

    Chapter  Google Scholar 

  • Leins P, Erbar C (2010) Flower and fruit: Morphology, ontogeny, phylogeny, function and ecology. Schweizerbart Science Publishers, Stuttgart

    Google Scholar 

  • Lima EA, Tölke ED, Silva-Luz CL, Demarco D, Carmello-Guerreiro SM (2021) Fruit morphoanatomy of Astronium Jacq. and Myracrodruon Allemão (Anacardiaceae): taxonomic implications and development of the calycinal wings. Braz J Bot. https://doi.org/10.1007/s40415-021-00732-w

    Article  Google Scholar 

  • Morton CM, Telmer C (2014) New subfamily classification for the Rutaceae. Ann Mo Bot Gard 99:620–641

    Article  Google Scholar 

  • Paoli AAS, Sarti J (2008) Morfoanatomia e desenvolvimento de frutos e sementes de Dodonea viscosa (L.) Jacquin (Sapindaceae). Rev Bras Sementes 30:33–42

    Article  Google Scholar 

  • Pirani JR (1998) A revision of Helietta and Balfourodendron (Rutaceae-Pteleinae). Brittonia 50:348–380

    Article  Google Scholar 

  • Pirani JR (1999) Estudos taxonômicos em Rutaceae: revisão de Helietta e Balfourodendron (Pteleinae). Análise cladística de Pteleinae. Sinopse de Rutaceae do Brasil. Habilitation thesis, Universidade de São Paulo, São Paulo

  • Pirani JR (2004) Three new species of Galipea (Rutaceae, Galipeinae) from Brazil. Bot J Linn Soc 144:365–373

    Article  Google Scholar 

  • Pirani JR (2005) Flora da Reserva Ducke, Amazonas, Brasil: Rutaceae. Rodriguésia 56:189–204

    Article  Google Scholar 

  • Pirani JR, Kallunki JA (2007) Two new species of Galipea (Rutaceae, Galipeae) from Bolivia, Ecuador, and Peru. Brittonia 59:343–349

    Article  Google Scholar 

  • Pirani JR, El Ottra JHL, Menezes NL (2010) Morfoanatomia da flor de cinco espécies de Galipea Aubl. e seu significado na evolução de flores tubulosas entre as Rutaceae neotropicais. Rev Bras Bot 33:301–318

    Article  Google Scholar 

  • Pirani JR, Groppo M (2020) Rutaceae in Flora do Brasil 2020. Jardim Botânico do Rio Janeiro. http://reflora.jbrj.gov.br/reflora/floradobrasil/FB212. Accessed 8 Jun 2021

  • Porter DM, Elias TS (1979) Flora of Panama. Part VI. Family 89. Rutaceae Ann Mo Bot Gard 66:123–164

    Article  Google Scholar 

  • Radford AE, Dickison WC, Massey JR, Bell CR (1974) Vascular plant systematics. Harper & Row, New York

    Google Scholar 

  • Ramp E (1988) Struktur, Funktion und systematische Bedeutung des Gynoeciums bei den Rutaceae und Simaroubaceae. Ph.D. dissertation, Universität Zürich, Zürich

  • Roth I (1977) Fruits of angiosperms. Encyclopedia of plant anatomy. Vol. 10, Part 1. Gebrüder Borntraeger, Berlin

  • Roth I, Lindorf H (1972) Desarrollo y anatomía del fruto y de la semilla de Citrus. Acta Bot Venez 7:163–186

    Google Scholar 

  • Skorupa LA (1998) Three new species of Pilocarpus Vahl (Rutaceae) from Brazil. Novon 8:447–454

    Article  Google Scholar 

  • Skorupa LA (1999) A new species of Pilocarpus Vahl (Rutaceae) from Peru. Novon 9:257–259

    Article  Google Scholar 

  • Skorupa LA (2000) Espécies de Pilocarpus Vahl (Rutaceae) da Amazônia brasileira. Act Amaz 30:59–70

    Article  Google Scholar 

  • Skorupa LA, Pirani JR (2004) A new species of Pilocarpus (Rutaceae) from northern Brazil. Brittonia 56:147–150

    Article  Google Scholar 

  • Souza A, Mourão KSM, Souza LA (2005) Morfologia e anatomia do fruto e da semente em desenvolvimento de Pilocarpus pennatifolius Lem. (Rutaceae). Rev Bras Bot 28:175–184

    Google Scholar 

  • Souza LA, Moscheta IS, Mourão KSM, Rosa SM (2004) Morphology and anatomy of the flower and anthesis of Metrodorea nigra St. Hill. (Rutaceae). Braz Arch Biol Technol 47:107–112

    Article  Google Scholar 

  • Souza LA, Mourão KSM, Moscheta IS, Rosa SM (2003) Morfologia e anatomia da flor de Pilocarpus pennatifolius Lem. (Rutaceae). Rev Bras Bot 26:175–184

    Article  Google Scholar 

  • Souza LA, Rosa SM, Moscheta IS (2008) Anatomy of the developing fruit of Metrodorea nigra A. St.-Hil. (Rutaceae). Braz Arch Biol Technol 51:1171–1179

    Article  Google Scholar 

  • Spjut RW (1994) A systematic treatment of fruit types. Mem N Y Bot Gard 70:1–82

    Google Scholar 

  • Tölke EEAD, Lacchia APS, Demarco D, Carmello-Guerreiro SM (2017) Pericarp ontogeny of Tapirira guianensis Aubl. (Anacardiaceae) reveals a secretory endocarp in young stage. Acta Bot Bras 31:319–329

    Article  Google Scholar 

  • Van der Pijl L (1982) Principles of dispersal in higher plants, 3rd edn. Springer, Berlin

    Book  Google Scholar 

  • Weckerle CS, Rutishauser R (2005) Gynoecium, fruit and seed structure of Paullinieae (Sapindaceae). Bot J Linn Soc 147:159–189

    Article  Google Scholar 

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Acknowledgements

This work was supported by Grants from ‘Fundação de Amparo à Pesquisa do Estado de São Paulo’ (FAPESP; proc. #2014/18002‐2, #2015/09776-7 and #2018/14853-9), awarded to JRP, JHLEO and GOP, respectively. The first author was also granted with a short-term scholarship from National Council for Scientific and Technological Development (CNPq) (Grant ID: #144153/2018-1). We are grateful to Henrique Moreira for making a picture of a fruit of Hortia available for us. We also thank the technician of the Laboratory of Plant Anatomy (IB-USP) Tássia C. Santos, for her assistance to the first author in the laboratory.

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  1. Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, 05508-090, Brazil

    Guilherme de Ornellas Paschoalini, José Rubens Pirani, Diego Demarco & Juliana Hanna Leite El Ottra

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  1. Guilherme de Ornellas Paschoalini
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  2. José Rubens Pirani
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  3. Diego Demarco
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  4. Juliana Hanna Leite El Ottra
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GOP, JRP and JHLEO involved in conceptualization; GOP, JRP, DD and JHLEO took part in methodology; GOP, JRP, DD and JHLEO took part in formal analysis and investigation; GOP, JRP, DD and JHLEO involved in writing—original draft preparation; GOP, JRP, DD and JHLEO involved in writing—review and editing; GOP, JRP and JHLEO involved in funding acquisition; JRP and JHLEO took part in supervision. All authors have read and approved the final version of the manuscript.

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Correspondence to Guilherme de Ornellas Paschoalini or Juliana Hanna Leite El Ottra.

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Diego Demarco is the editor-in-chief of the Brazilian Journal of Botany, and this article was entirely handled by an associate editor.

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40415_2021_779_MOESM1_ESM.png

Fig. S1 Schematic drawings of anthetic gynoecium and fruit structure, including vasculature, in tribe Galipeeae at various ontogenetic stages. a–b Follicarium of Erythrochiton brasiliensis in two developmental stages (a, general view of carpels; b, detail of one mature fruitlet). c–e Capsule of Esenbeckia grandiflora in three successive developmental stages (c, general view of carpels; immature (d) and mature (e) fruits. f–g Samarium of Helietta glaziovii in two successive developmental stages (f, general view of carpels; g, immature fruit). h–j Capsule of Metrodorea nigra in three successive developmental stages (i, general view of carpels; h, immature fruit; j, detail of one mature fruitlet. Colors: light gray, vascular tissues; dark gray, endocarp. Line types: dotted lines, nectariferous disc; dashed lines, cut-line. (PNG 2494 KB)

40415_2021_779_MOESM2_ESM.docx

Table S1 Vouchers analyzed to compose the cladogram of Fig. 6 (DOCX 33 KB)

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Paschoalini, G.O., Pirani, J.R., Demarco, D. et al. Revisiting pericarp structure, dehiscence and seed dispersal in Galipeeae (Zanthoxyloideae, Rutaceae). Braz. J. Bot 45, 415–429 (2022). https://doi.org/10.1007/s40415-021-00779-9

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